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First Examination of Diet Items Consumed by Wild-Caught Black Carp (Mylopharyngodon piceus) in the U.S.

INTRODUCTION

The number of introduced freshwater fish species considered invasive or alien in the U.S. has increased in the last 20 y, with several species classified as injurious to native aquatic fauna (Neilsen and Fuller, 2017; NISIC, 2005). The four most economically important carp species native to eastern Asia (grass carp Ctenopharyngodon idella, bighead carp Hypophthalmichthys nobilis, silver carp H. molitrix and black carp Mylopharyngodon piceus; Yi et al, 1988) are now well established in the U.S. (Chapman and Hoff, 2011). These four species, known in China as the si da jia yu (four large domestic fishes; Kocovsky et al., 2018), are among the most economically important fishes in the world because of their extensive cultivation as fish food (IHAS, 1976; Tang, 1970; Roberts et al., 1973; Chang, 1987), and for biological control (Leventer and Teltsch,1990; Hickling, 1971; Ling, 1977). However, introductions of these species have caused detrimental ecological effects in Europe and North America, outside their native range in China and eastern Russia (Irons et al, 2007; Haupt and Phelps, 2016; Milardi et al, 2017; Chang, 1966; Evtushenko et al, 1994). In 2007 black carp was listed as an injurious fish under the Lacey Act (USFWS, 2007). Although black carp were first imported in the 1970s (Nico et al, 2005), the effects of its introduction on the ecology of large river systems is the least known of the four species because it has taken the longest for wild populations to become established in the U.S. (Nico and Jelks, 2011) and because most published research on black carp is based on fish in aquaculture (Collins, 1996; El-Deeb and Ismail, 2004; Nico et al, 2005; Kelly, 2011). Aquaculture facilities in the U.S. acquired black carp as a biological control agent because of their ability to consume large numbers of snails that are intermediate hosts of parasites, such as the yellow grub (Clinostomum margaritum) that infect catfish and other cultivated food fish (Nico et al., 2005). Black carp presumably escaped into the wild from these facilities (Nico et al, 2005), with the first wild-caught black carp officially reported from Illinois in 2003 (Chick et al, 2003). However, Nico et al (2005) indicated commercial fishers in Louisiana may have captured black carp in hoop nets on numerous occasions since the 1990s.

A unique characteristic of black carp is their extensively developed pharyngeal teeth (adapted for crushing mollusks), which have been well-characterized and studied (e.g. Liu et al, 1990; Shelton et al, 1995; He et al, 2013). Hung et al (2015) reported that teeth of carp and other cyprinids are shed during growth and replaced by new teeth with increased hardness. The chronological development of molariform teeth in this species is commensurate with changes in diet as they age. Their diet changes from zooplankton and small invertebrates in the first year of life to larger invertebrates and mollusks at about 110 mm total length (TL) when their pharyngeal teeth develop to crush shells (Liu et al, 1990; Hung et al, 2015). Laboratory feeding studies indicate consumption of mollusks is related to mouth gape and the ability to crush shells (Shelton et al, 1995).

Nico et al. (2005) comprehensively summarized available information on black carp and more recently provided an update on the status of this species in North America (Nico and Jelks, 2011). Although black carp are often described as nearly obligatory bottom-feeding molluscivores, Nico et al (2005) indicates a wider variety of invertebrate diet items and flexibility in foraging behavior. Such flexibility and opportunism in feeding could contribute to the future success of this species in North America. Diet and feeding characteristics of black carp have been studied in culture ponds and the laboratory (summarized by Nico et al, 2005; Ledford and Kelly, 2006); however, larger fish (>320 mm TL) have not been tested. Few diet studies on wild black carp have been conducted, partially because wild populations in their native range have declined (Nico et al., 2005). To date no examination of diet, foraging behavior, or habitat use in wild fish has been conducted in the U.S., even though reproductively active populations of this species are now likely established in the Mississippi River basin (Nico et al, 2005). As of October 2018, approximately 300 black carp catches have been documented. Even though reports of wild black carp in the Mississippi River drainage have increased and captures by commercial fishers are now a regular occurrence, we suspect most captures of black carp from the southern U.S. are unreported, in part due to their similarity in appearance with grass carp. Because this species primarily feeds on mollusks, the risk of an increasing population to native aquatic fauna is of serious concern, and diet information is critical to understand current effects on ecosystems and endangered mollusks. It is estimated 65% of unionid mussel species (Haag and Williams, 2014) and 64% of freshwater gastropod species (Johnson et al., 2013) have some level of imperilment. Nico et al. (2005) previously noted in North America, black carp have the potential to occupy an ecological niche no other freshwater fish species currently fills, that of a molluscivore inhabiting large rivers with the ability to feed on a wide variety of diet items, attain large size (over 1 m TL and > 50 kg), and exhibit high growth rates and fecundity under favorable conditions.

The purpose of this study was to inventor)' diet items consumed by wild black carp to gather critical knowledge on the feeding ecology, behavior, and habitat use of this species that may help guide future management, control, and risk assessment to native fauna. Nico et al. (2005) recognized diet information on wild fish was an information gap among the previously published research. Our specific objectives were to create a taxonomic list of diet items consumed by wild-caught fish, report the spatial and temporal distribution of samples, and summarize functional associations between diet items consumed and feeding ecology of this species.

MATERIALS AND METHODS

STUDY AREA

Specimens of wild-caught black carp were provided for examination over an 8 y period (2009-2017) as part of a collaborative research project between federal and state agencies and universities. The program consisted of outreach to commercial fishers and a bounty system issued by the state of Illinois for fish captured within Illinois waters and those of contiguous states. Additional collections were contracted from commercial fishers within reaches of the Mississippi and Atchafalaya rivers where previous reports of black carp had occurred. State agencies and universities also provided captures by biologists throughout the species range. Fish were acquired to obtain data on the range expansion and distribution of black carp, including verification of species, capture locations and methods, determination of age, timing and status of reproductive potential, trophic status, individual specimen origin (wild versus hatchery), and diet analysis. This paper includes results from the diet analysis, which consisted of samples collected from 109 wild-caught black carp captured in the Mississippi River basin from both riverine and off-channel habitats with slack water, including sloughs, oxbow lakes, and reservoirs. The geographic range of the fish obtained includes the Mississippi River mainstem and the Atchafalaya, Cumberland, Illinois, Kaskaskia, Ohio, and White River drainages (Fig. 1). The geographic extent of fish capture locations encompasses an area bound by the following coordinates (latitude and longitude, respectively): north extent 40.9371N, -89.45242W, south extent 30.994973N, -91.773392W, east extent 37.0083825N, -88.2105405W, and west extent 30.994973N, -91.773392W. Specific capture locations of black carp specimens are available at https:// doi.org/10.5066/P9K88CWF.

LABORATORY PREPARATION

Black carp were either previously frozen or transported dead on ice to the Columbia Environmental Research Center (CERC; Columbia, Missouri) for removal of gastrointestinal (GI) tracts. The entire GI tract was removed and contents preserved in 10% neutral buffered formalin until sorting. Samples were sorted under microscopes to remove all organisms, including whole and partial individuals (i.e. invertebrate appendages, mollusk shell fragments) and plant matter. Upon sorting all contents were transferred to 80% ethanol, then enumerated and identified to the lowest practical taxonomic unit with a dissecting microscope. Mollusks were identified to various taxonomic levels depending on the degree of shell fragmentation and recovery of diagnostic shell structures in the gut (i.e. hinge teeth, cardinal teeth, and beak sculpture of Unionids; opercula and radula of Gastropods). When fragmentation, the mastication, and or partial digestion of mollusks prevented exact counts, abundance was estimated if possible based on mollusk shell pieces and presence of diagnostic structures. For fish that contained at least five intact shells (whole or nearly so) of the same snail taxa, we measured length (tip of spire to edge of aperture, in millimeters) to provide an approximate size range.

Larval midge specimens (Diptera: Chironomidae) were mounted on labeled glass slides with CMCP-10 mounting media (Masters Chemical Co., Des Plaines, Illinois) and allowed to cure for 1 mo before identification with the use of a compound microscope. Macroinvertebrate organisms were identified to the lowest practical taxonomic level using various keys. Trematoda (flukes) were stained and mounted on glass slides for species identification with electron microscopy, based on descriptions by Fuller (1974) and Alves et al. (2015). Standard taxonomic references were used for insect identification (Merritt et al, 2008), and most noninsect macroinvertebrates (Pennak, 1989; Thorp and Covich, 2001). Unionid mussels were identified via Oesch (1984), McMahon and Bogan (2001), Cummins and Mayer (1992), and McMurray et al (2012). Snails (Gastropoda) were identified via Burch (1982) and Brown (1991) and regional keys of riverine species (Wu et al., 1997). Voucher specimens of all macroinvertebrate taxa were retained for verification purposes.

DATA ANALYSIS

Due to the varied condition of diet specimens which resulted in different levels of taxonomic identification, we relied on percent (%) incidence for comparisons in this study, which is defined by Buckland et al (2017) as the percentage of total fish examined that contained a specific diet item or taxonomic group. Incidence was determined for each individual taxon, general taxon groups (ex. mollusks, bivalves, snails, insects, and other invertebrates), and specific groups of interest such as zebra mussels (Dreissena) and Asian clams (Corbicula) which were identified only to genus-level because of taxonomic revisions and ongoing genetics research. Capture locations for each individual fish were classified as lotic (mainstem flowing water habitats, including side channels and chutes) or lentic (offchannel areas, including backwater sloughs, oxbows, or reservoirs). For each GI tract sample, taxonomic richness (number of distinct taxa) among diet items consumed was qualitatively compared. We compared taxonomic richness of diet items between fish collected in lentic and lotic habitats using a Rruskall-Wallis/Mann-Whitney U test.

RESULTS

Black carp included in this study consisted of 51% hoop net, 13% gill net, and 33% unreported capture methods; individual (1 each) electrofishing, rotenone, and trammel net captures were also reported. Captures were distributed among the three segments (including side-channels and backwaters) of the Mississippi River (MR); with the upper MR including the inter-dam reaches upstream of lock and dam 26 (the lowest dam on the Mississippi River near Alton, IL; 7%), middle MR from lock and dam 26 to the confluence of the Ohio River (37%), and the lower MR downstream of the confluence of the Ohio River to the Gulf of Mexico (34%). Additional captures were provided from the Atchafalaya, Cumberland, Illinois, Kaskaskia, Ohio, and White river drainages (Fig. 1). Captured black carp ranged from 410-1312 mm total length (Fig. 2), and most were captured during the summer months of June-Sept. (Fig. 3).

Of 109 black carp examined, 60 contained identifiable items, 31 were empty, and 18 only contained the fluke Aspidogaster conchicola Baer, 1827 (Trematoda: Aspidogastridae, Fig. 3). We identified 59 animal taxa, including 21 mollusks, 27 insects, and 11 other noninsect invertebrates (Table 1). The highest incidence was observed in insects (37.6%) and mollusks (26.6%), with the most frequently ingested groups: snails (Gastropoda), caddisflies (Trichoptera), mussels (Unionidae), and aquatic midges (Diptera: Chironomidae).

Of mollusks present, snails were found in 16.5% of the fish examined (Fig. 4). Only eight fish examined had numerous intact gastropod shells that could be measured and identified (> five individuals of the same taxa), and the proportion of shells found in those fish that were crushed or fragmented varied considerably (from zero to 80%; Table 2). Bivalve mollusks were present, with 13.7% incidence for unionids, 5.5% for zebra mussels, and 3.7% for Asian clams (Fig. 4). Unlike gastropods, bivalve shells were usually fragmented and incomplete, complicating identification and enumeration. Nevertheless, six samples had shell fragments with diagnostic characters needed for identification of unionids. Among these, seven taxa were identified, and individual fish consumed up to four unionid species (Table 3).

Among the insects found (Fig. 4), caddisflies (Trichoptera) had the highest incidence (15.6%) followed by aquatic midges (Chironomidae, 13.7%) and mayflies (Ephemeroptera, 6.4%). All caddisflies were net-spinning taxa (Family Hydropsychidae) and in low abundance (< 10 individuals; Table 1). The highest abundance of aquatic midges was consumed by fish from lentic habitats (Table 4), with Glyptotendipes and Dicrotendipes the two most abundant taxa. The most commonly encountered mayflies were burrowing species associated with sediments (families Ephemeridae and Pentageniidae), although a 761 mm fish captured from the Illinois River during the annual hatch of Hexagenia mayflies had consumed 30 winged H. bilineata (subimago and imago).

Other taxa ingested by fish examined include freshwater sponges (Porifera), crustaceans (Ostracoda and Decapoda), water mites (Acarina), and four worm phyla (Table 1). All flukes (33%) were identified as Aspidogaster conchicola. In 17% of fish examined, these flukes were the only diet item found in the GI tract (Fig. 3).

Black carp also consumed additional invertebrate taxa in low incidence that were not previously reported in other studies (Table 1), including freshwater sponges, water mites, three groups of worms (Phyla Nemertea, Nematoda, and Annelida in Class Hirudinea), beetles (Coleoptera), springtails (Collembola), blackfly larvae (Diptera: Simulidae), and Lepidoptera (Pyralidae).

Several fish consumed large numbers of only one or two taxa; we observed >10 individuals (range in abundance of 11 to 108 individuals) for Viviparus snails (six fish), chironomids (five fish), Pleurocera snails (two fish), zebra mussels (two fish), water mites (one fish), Ostracoda (one fish), and Corbicula (one fish). Several fish contained plant-based organic detritus, which may have been ingested accidentally during benthic foraging. Three carp ingested duckweed (Lemna), and two of those also consumed large numbers (>100) of chironomid midges. Nine samples contained unidentifiable crushed nut or seed fragments, but three additional fish ingested pecan nuts (Carya illinoinensis), evidenced by large shell pieces and fragmented meat.

Insects (27 taxa) and mollusks (21 taxa) had the highest richness (number of diet taxa) of diet items (Fig. 4). Mean diet richness was 1.9, and individual fish consumed as many as 11 items. Fish captured in lentic habitats consumed a significantly greater richness (mean 5.2) than fish caught in lotic habitats (mean 1.3) based on Kruskal-Wallis/Mann-Whitney U test (n = 109, adjusted H = 23.4, P < 0.01, Fig. 5). Two diet groups were exclusive to capture habitat: all fish consuming viviparid snails were from lentic habitats, and all fish consuming Trichoptera were from lotic habitats (Fig. 4).

DISCUSSION

This study represents the first inventory of diet items from wild-caught black carp in the U.S. and constitutes the largest sample size of black carp diets, with the previous largest study on wild fish consisting of nine individuals collected from the Amur River in China (Nico et al., 2005). Further, our study consisted of larger fish (>400 mm) than those examined in black carp diet studies with cultured fish, so data presented is not previously reported diet information. However, there are some limitations regarding how these data can be interpreted. Most black carp were captured by commercial fishers targeting other species. Therefore, capture locations and fish sizes are biased for collection methods and susceptibility to gear (Fig. 2). Furthermore, the multiple seasons of capture, variability in time fish spent in nets prior to harvest (1-4 d in hoop nets, the most commonly employed gear) and in transit to the laboratory, can result in variable condition of gut contents. Crushed or partially crushed diet items remaining in the guts varied considerably in both condition and completeness, and the resulting variable levels of taxonomic identification complicate quantification of diet items.

Among the black carp diet studies summarized by Nico et al. (2005), only two were conducted in the U.S., where taxa in gastropod families Physidae and Planorbidae were consumed by juvenile fish in aquaculture ponds. Including these, we observed 15 taxa that were also listed in Nico et al. (2005) as diet items consumed across Eurasia (Table 1), where gastropods were the most frequently reported. This also included Viviparus river snails (Viviparidae) which were reported in the Amur River basin (Nico et al., 2005). Several authors reported insect taxa as diet items (summarized in Evtushenko et al., 1994; Nico et al., 2005). Aquatic midges (Chironomidae) were commonly reported as a diet item (Nico et al., 2005), and these organisms had the second highest incidence of any insect group in our samples (13.7%, Fig. 4). Ostracoda and other microcrustaceans that include zooplankton have been reported in the diet of larval and juvenile black carp (Evtushenko et al., 1994; Nico et al., 2005), and we also observed ostracods (<1%) and bryozoans (2.7%). Since these previous studies included smaller wild or hatchery fish, our study is the first to report ingestion of these smaller diet items by larger fish (>400mm TL). Larger crustaceans such as crayfish (Decapoda) were reported in the diet by several studies (Nico et al., 2005); we found remnants of crayfish in only one wild fish, though adult-sized black carp will readily consume live crayfish in captivity (D. Chapman, pers. observ.). In addition to the native unionid (13.7%) and sphaeriid (1.8%) bivalves, zebra mussels and Asian clams were also consumed as diet items in our study. Nico et al. (2005) noted black carp consume zebra mussels in culture ponds, but were uncertain black carp would prefer to consume zebra mussels in the wild, because of their tendency to form "rafts" when they attach to hard substrates or each other (Lewindowski, 1982), making them difficult to dislodge. In comparison to other mollusks, only a small percent of our fish consumed zebra mussels (5.5%) or Asian clams (3.7%), but some individual fish consumed an abundance of these prey items. In a 757 mm fish that consumed over 100 zebra mussels, the presence of numerous byssal threads suggests black carp can dislodge them from a substrate surface. Overall, native invertebrate taxa composed a higher percentage of diet items than nonnative mollusks. We found flukes (Aspidogaster conchicola) in many fish, including 18 samples where these organisms were the only diet taxa found. This fluke parasitizes numerous mollusk taxa in North America (Fuller, 1974; Alves et al., 2015), including viviparid snails and zebra mussels (Laruelle and Mollogy, 1996). Literature indicates these flukes will remain in the gut of fish species after the host mollusk has been digested (Evtushenko et al., 1994). Even though these flukes were not intentionally consumed by black carp, we have treated them as a diet item because they are an indicator of prior ingestion of parasitized mollusks. The high incidence of flukes (33%) provides further evidence that black carp are molluscivorous in the wild.

These black carp consumed taxa not previously reported (Table 1), including freshwater sponges, water mites, three groups of worms (Phyla Nemertea, Nematoda, and Annelida in Class Hirudinea), beetles, springtails, blackfly larvae, and Lepidoptera larvae. These taxa were found in low enough incidence that they could have been consumed accidentally while feeding on other benthic organisms (Table 1), especially those found in subsurface layers of sediment or attached biofilms that are associated with benthic substrates. Caddisfly (Trichoptera) larvae had not previously been reported in the diet of black carp but had the highest incidence of any insect group (15.6%). All caddisflies belonged to one family of filter-feeders (Hydropsychidae) and were from fish captured in lotic habitats. Previous studies summarized by Nico et al. (2005) included unidentified insect larvae in the diet of fish in lotic waters but did not report any filter-feeding insects. Of the 16 fish containing caddisflies, 11 were captured with hoop nets and had < 10 caddisflies per individual, therefore it is possible these organisms were ingested while fish were in the net. There has been no evidence black carp consume fish as a diet item, either referenced in Nico et al. (2005) or in our samples.

Nico et al. (2005) noted black carp as a gape-limited predator, and previous literature suggests that variability in degree of shell crushing or mastication of prey may be a function of fish size (measured by total length or mouth gape) in relation to the shape, size and texture of individual diet items (Shelton et al., 1995; Hung et al., 2015). The variability in percent of crushed shells in both slender-shaped Hornsnails (Pleuroceridae, 0-80%) and more globular shaped river snails (Viviparidae, 3-65%) that we observed (Table 2) supports the premise that black carp can detect size and shape of gastropod diet items. In soft-bodied prey items such as insect larvae, El-Deeb and Ismail (2004) found only insect parts in the guts of smaller cultivated fish (<250mm TL), implying possible mastication of these organisms. In contrast, a 1020 mm fish we examined had consumed several whole burrowing mayfly nymphs with no indication of mastication. This finding appears to support their ability to detect the texture of diet items as well as size. Even though mouth gape measurements were not available for many fish, the relationship between mouth gape and total fish length established by Nico et al. (2005) implies the gape of our smallest fish to be >25mm, larger than many gastropods consumed by the fish (Table 2). This is consistent with our observations of black carp consuming multiple snails without crashing the shells, and consumption of soft-bodied mayfly nymphs without any mastication.

In contrast to gastropods where many shells were intact after ingestion, unionid mussels were masticated and crashed to the point where only small shell fragments remained in the gut. It has been noted in tank studies that black carp can expel, rather than swallow, a portion of the shell fragments after crushing bivalves (P. Kroboth, pers. observ.). Seven black carp had ingested unionid mussels contained shell fragments which could be identified to species (Table 3), but much of the shell was missing in those samples. Nico et al. (2005) reported two wild black carp from the Amur River basin consumed unionid mussels. Evtushenko et al. (1994) also reported that in the Amur River, black carp consume Cristaria plicata (Leach, 1815), a winged unionid with a moderately thin shell (Zhadin, 1952) similar to the pink heelsplitter (Potamilus alatus), a Mississippi River basin species found in our study. As only a few shell fragments remained in more than half the fish that consumed unionids (eight of 15 total), it is possible the abundance and importance of unionid mussels in the diet of black carp may be underestimated.

Over a hundred midges (Chironomidae) were consumed by fish captured in lentic habitats and were also present, in lower abundance, among fish captured in lotic habitats (Table 4). Evtushenko et al. (1994) reported midges in the diet of smaller black carp (<250 mm TL), but the consumption of these organisms by wild fish in the Amur River reported by Nico et al. (2005) did not specify fish sizes for comparison. The most common midges identified in our fish were Glyptotendipes and Dicrotendipes, both of which are known to inhabit sediments in nutrient-rich lentic habitats (Saether, 1979). Most aquatic midge larvae of these taxa are small (<10 mm), indicating large black carp are capable of ingesting these and other small organisms in abundance. It is possible black carp possess the ability to sort through bottom substrates by sifting food items prior to ingestion, a strategy reported for common carp Cyprinus carpio (Sibbing, 1988) that may result in more efficient consumption of small prey items.

Our results indicate black carp can capitalize on specific diet items, because several fish had consumed larger numbers (>10 individuals) of only one or two taxa. Nico et al. (2005) noted one study reported wild black carp will consume large numbers of 1-2 gastropod taxa in the Amur River. In our study larger numbers (>10) of zebra mussels, Asian clams, water mites, seed shrimp, snails (Table 3), and chironomids (Table 4) were ingested by individual black carp. In addition two black carp also consumed multiple burrowing mayflies, including Hexagenia nymphs (eight in one fish), and winged stages of H. bilineata (30 in one fish). The bioenergetics model developed by Hodgins et al. (2014) for cultured black carp predicts consumption of diet items in large numbers, particularly for mollusks. Occurrence of diet items across seasons and capture locations suggest these are likely consumed intentionally, but it is possible some organisms reported in Table 1 with low percent incidence and abundance may have been ingested accidentally during benthic feeding. Diet availability studies conducted in the wild as well as laboratory feeding experiments with black carp are needed for further interpretation of these results.

Invertebrate diet items were identified to the lowest practical taxonomic level to assess casual associations between diet items and feeding modes utilized by black carp. Shelton et al. (1995) suggests black carp are reluctant to feed on the surface, but this may be an artifact of laboratory conditions, and not indicative of feeding behavior in the wild. We found free-swimming invertebrates and those found at or near the water surface were also consumed by black carp, including water boatmen (Hemiptera: Corixidae), aquatic beetles (Berosus), and adult mayflies during their emergence. Duckweed found in our fish also indicates occasional feeding at or near the surface. Ben-Ami and Heller (2001) demonstrated the ability of black carp to feed on sediment burrowing organisms, confirmed by the presence of burrowing mayfly nymphs and numerous sediment-dwelling chironomids (Table 4). The presence of plant material, also reported in juvenile black carp in China (Nico et al., 2005), provided additional evidence of benthic feeding. However, no studies had documented active consumption of plant material by black carp in the wild. Nuts and seeds (such as pecans) may be ingested after entering the water or becoming submerged, as these plant parts may match the black carp's search image for a mollusk forage. The observation of nuts and seeds along with a high percent incidence of detritus (29.3%) among diet samples suggest black carp may disperse plant seeds, as observed in common carp (Von Bank et al, 2018). Taken together, results indicate black carp ingest both plant and invertebrate diet items and are capable of feeding on small sediment-dwelling organisms, in the mid-water column, and occasionally at the surface.

Consumed taxa inhabit different flow regimes and substrates, providing evidence black carp feed in multiple habitats. Fish captured in lentic habitats consumed a significantly higher number of taxa (Fig. 5). Lentic habitats of the Mississippi River basin are known to contain higher energy food sources than lotic habitats (Eggleton and Schramm, 2004) implying black carp may spend more time foraging in off-channel habitats. However, among the fish that consumed unionid mussels (n = 15), eight were captured in lotic habitats and seven in lentic habitats, indicating that black carp fed on mussels in both environments. Unionid species identified in this study are somewhat generalists in their substrate and habitat preferences, inhabiting backwaters with soft mud or low-velocity margins of riverine habitats with sand or silt bottom substrates (Oesch, 1984; McMurray et al., 2012). Snails were also ingested in abundance by black carp in both habitats. Focused research comparing food availability and selection among habitats will be required to determine ecosystem effects and competition with native species.

Documentation of unique and previously unreported diet items, propensity to consume multiple individuals of the same diet taxon, and consumption of species that occupy various depths in the water column, contribute valuable knowledge to understanding of black carp feeding ecology. Additional taxa collected in future examinations from range expansions where habitats, substrates, and invertebrate taxa differ, combined with cumulative observations of diet items consumed within the current species range, may add weight to the observations of this study. Our results highlight the need for additional laboratory feeding studies with diet items of various sizes and shapes to determine gape limitations, gut evacuation rates, and expulsion of shell fragments during and after ingestion. Conclusions of our study provide a foundation for trophic research with stable isotopes (Nico andjelks, 2011; H. Evans, pers.comm.). We recognize the need for habitat-use data not biased by capture methods, and the value that may be contributed by future diet studies with wild juvenile fish of smaller sizes (<400 mm TL) or very large adult specimens (>1.5 m TL), neither of which were included among fish in this study.

This study provides a qualitative snapshot of diet items consumed by wild black carp throughout the current species distribution in the U.S. and documents the extent to which these fish feed on native mollusks, other aquatic invertebrates, and invasive species such as zebra mussels and Corbicula. Recent black carp records in the greater Mississippi River drainage indicate this species is still in the process of population increase and range expansion (Nico and Jelks, 2011). Further, consumption rates for cultured black carp (Hodgins et al, 2014) indicate this species has the potential to rapidly deplete native mollusks, and localized or fragmented populations may be particularly vulnerable. The Mississippi River basin supports higher densities and up to four times as many unionid species as the most diverse freshwater systems of other continents (Haag, 2012; Haag and Williams, 2014), and larger tributaries where recent black carp captures have been reported also have a rich diversity of native mollusks with many imperiled species (Buchanan, 1980; Lydeard et al., 2004). One species in our samples, purple lilliput (Toxolasma lividum), is currently being assessed for prelisting under the Endangered Species Act (J. Hundley, USFWS, pers. comm.). For freshwater snails in flowing waters, most imperiled species are located further upstream in headwater reaches (Johnson et al., 2013), but the risk black carp will invade smaller watersheds is currently unknown because most black carp captures are by commercial fishers that do not operate in these systems.

Collectively, higher incidence of mollusks and insects in our samples as compared to other diet taxa and the consumption of a wide variety of invertebrates across several different animal phyla support the classification of black carp as a benthic foraging invertivore. Ingestion of plant matter and invertebrate taxa that occupy non-benthic zones of the water column suggests black carp are flexible in their feeding modes. The conclusion of Nico et al. (2005) that black carp are opportunistic was based mainly on culture studies with smaller fish (<320 mm TL), but diet composition of larger wild fish also supports this classification. Our results documenting the breadth of taxa consumed by wild black carp, ingestion of high abundances of a single diet taxon, and multiple species of unionid mussels that inhabit both lentic and lotic habitats, confirm that the invasion of this species poses a risk to native aquatic fauna in the U.S.

[Please note: Some non-Latin characters were omitted from this article]

Acknowledgments.--We thank Shannon Amiot, Anne Herndon, and Lauren Mott for assistance with laboratory processing and data preparation. The authors also thank the numerous commercial fishers who provided fish for this study, and biologists who collected specimens. We also thank Kelly Baerwaldt of the U.S. Fish and Wildlife Service, Nate Hodgins of the Minnesota Dept. of Natural Resources, and two anonymous reviewers for their helpful suggestions regarding earlier versions of the manuscript. This study was partially funded through the Great Lakes Restoration Initiativ e and the U.S. Geological Survey, ecosystems mission area. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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SUBMITTED 29 OCTOBER 2018 ACCEPTED 3 APRIL 2019

DATA AVAILABILITY STATEMENT

Data associated with this study will be made publicly available at the following pre-reserved DOI link:

https://doi.org/10.5066/P9K88CWF

B.C. POULTON (1), P.T. KROBOTH, A.E. GEORGE, AND D.C. CHAPMAN U.S. Geological Survey, Columbia Environmental Research Center, Columbia, Missouri 65201

J. BAILEY US Fish and Wildlife Service, La Crosse Fish Health Center, 555 Lester Ave, Onalaska, Wisconsin 54650

AND

S.E. MCMURRAY AND J.S. FAIMAN Missouri Department of Conservation, Conservation Research Center, 3500 East Cans Rd., Columbia 65201.

(1) Corresponding author: Telephone: 573- 876-1873; Fax: 573-876-1863; E-mail: bpoulton@usgs.gov

Caption: FIG. 1.--Capture locations of black carp examined in ibis study from the Mississippi River drainage (n=109). Black triangles indicate lentic habitat and gray squares indicate lotic habitat

Caption: FIG. 2.--Length-frequency of wild-caught black carp captured from the Mississippi River basin in 20092017 that were examined for diet items consumed (n=109). Frequency represents number of fish examined in each of the 50 mm size groupings

Caption: FIG. 3.--Frequency (n=109), by month of capture from the Mississippi River basin in 2009-2017) of wild-caught black carp gastrointestinal tracts examined that were empty (no identifiable contents), contained flukes only (Aspidogaster conchicola), and had other identifiable diet items present

Caption: FIG. 5.--Plot of mean taxonomic richness (number of distinct taxa) of diet items consumed by wildcaught black carp captured from lentic and lotic habitats in the Mississippi River drainage in 2009-2017. Error bars represent one standard deviation of means
TABLE 1.-Identification of diet items consumed
by wild-caught black carp captured 2009-2017, and
classification of consumption (ingestion status) based
on percent incidence (% of fish examined; plant material
excluded): A = likely diet item (mollusks, and other taxa
with % incidence >5); B = probable diet item with percent
incidence >5 and low abundance (< 10 individuals);
C = taxa with percent incidence <1 nd low abundance
(<5 individuals) and/or presence may indicate accidental
consumption while ingesting other taxa: D = taxonomic
identification limited due to level of digestion or
fragmentation. An asterisk (*) indicates taxon also
reported in Appendix 2 of Nico et al., (2005)

Animal group                                 Reported as
                                             (lowest taxonomic
                                             unit possible)

Porifera--Freshwater Sponges                 Porifera
Turbellaria--Flukes                          Aspidogaster conchicola
Nematoda--Roundworms                         Nematoda (unkeved)
Nemertea--Ribbonworms                        Prostoma
Bryozoa *--Moss animals                      Plumatella
Annelida *--Segmented worms                  Oligochaeta
Hirudinea--Leeches                           Erpobdellidae
Mollusca--Snails and Clams                   Mollusca *
Mollusca--Asian Clam                         Corbirula *
Mollusca--Zebra Mussel                       Dreissena *
Mollusca--Unionidae (Freshwater bivalves)    Unionidae *
Mollusca--Unionidae                          Arcidens confragosus
Mollusca--Unionidae                          Leptodea fragilis
Mollusca--Unionidae                          Potamilus alatus
Mollusca--Unionidae                          Pyganodon grandis
Mollusca--Unionidae                          Toxolasma lividum
Mollusca--Unionidae                          Toxolasma
Mollusca--Sphaeriidae (Fingernail Clams)     Musculium
Mollusca--Gastropoda (Snails)                Gastropoda *
Mollusca--Lymnaeidae                         Lymnaeidae
Mollusca--Physidae                           Physella *
Mollusca--Planorbidae                        Planorbidae
Mollusca--Pleuroceridae                      Pleuroceridae
Mollusca--Pleuroceridae                      Pleurocera acuta gp.
Mollusca--Viviparidae                        Viviparidae *
Mollusca--Viviparidae                        Viviparus *
Mollusca--Viviparidae                        Viviparus subpurpureous
Crustacea--Decapoda *                        Cambaridae
Crustacea--Ostracoda                         Ostracoda *
Arachnida--Acarina                           Acarina
Insecta *                                    Insecta
Insecta--Coleoptera (Beetles)                Carabidae
Insecta--Coleoptera                          Berosus
Insecta--Collembolla (Springtails)           Collembola
Insecta--Diptera (True Flies)                Diptera (unkeyed)
Insecta--Simulidae (Black flies)             Simulium
Insecta--Chironomidae (Non-biting Midges)    Chironomidae *
Insecta--Chironomidae                        Axarus
Insecta--Chironomidae                        Chironomus
Insecta--Chironomidae                        Coelotanypus
Insecta--Chironomidae                        Dicrotendipes
Insecta--Chironomidae                        Glyptotendipes
Insecta--Chironomidae                        Parachironomus
Insecta--Chironomidae                        Polypedilum
Insecta--Chironomidae                        Saetheria
Insecta--Ephemeroptera (Mayflies)            Ephemeroptera *
Insecta--Ephemeroptera                       Caenis
Insecta--Ephemeroptera                       Hexagenia
Insecta--Ephemeroptera                       Hexagenia bilineata
Insecta--Ephemeroptera                       Pentagenia
Insecta--Hemiptera * (True lings)            Corixidae
Insecta--Hemiptera                           Palmacorixa
Insecta--Lepidoptera (Moths)                 Pyralidae
Insecta--Trichoptera (Caddisflies)           Hydropsychidae
Insecta--Trichoptera                         Cheumatopsyche
Insecta--Trichoptera                         Hydropsyche
Insecta--Trichoptera                         Hydropsyche orris
Insecta--Trichoptera                         Potamyia flava

Animal group                                 Ingestion
                                              status

Porifera--Freshwater Sponges                     C
Turbellaria--Flukes                              C
Nematoda--Roundworms                             C
Nemertea--Ribbonworms                            C
Bryozoa *--Moss animals                          C
Annelida *--Segmented worms                      C
Hirudinea--Leeches                               C
Mollusca--Snails and Clams                       D
Mollusca--Asian Clam                             A
Mollusca--Zebra Mussel                           A
Mollusca--Unionidae (Freshwater bivalves)        D
Mollusca--Unionidae                              A
Mollusca--Unionidae                              A
Mollusca--Unionidae                              A
Mollusca--Unionidae                              A
Mollusca--Unionidae                              A
Mollusca--Unionidae                              A
Mollusca--Sphaeriidae (Fingernail Clams)         A
Mollusca--Gastropoda (Snails)                    D
Mollusca--Lymnaeidae                             A
Mollusca--Physidae                               A
Mollusca--Planorbidae                            A
Mollusca--Pleuroceridae                          A
Mollusca--Pleuroceridae                          A
Mollusca--Viviparidae                            A
Mollusca--Viviparidae                            A
Mollusca--Viviparidae                            A
Crustacea--Decapoda *                            D
Crustacea--Ostracoda                             C
Arachnida--Acarina                               C
Insecta *                                        D
Insecta--Coleoptera (Beetles)                    A
Insecta--Coleoptera                              A
Insecta--Collembolla (Springtails)               C
Insecta--Diptera (True Flies)                    C
Insecta--Simulidae (Black flies)                 C
Insecta--Chironomidae (Non-biting Midges)        D
Insecta--Chironomidae                            A
Insecta--Chironomidae                            A
Insecta--Chironomidae                            A
Insecta--Chironomidae                            A
Insecta--Chironomidae                            A
Insecta--Chironomidae                            A
Insecta--Chironomidae                            A
Insecta--Chironomidae                            A
Insecta--Ephemeroptera (Mayflies)                D
Insecta--Ephemeroptera                           C
Insecta--Ephemeroptera                           A
Insecta--Ephemeroptera                           A
Insecta--Ephemeroptera                           A
Insecta--Hemiptera * (True lings)                C
Insecta--Hemiptera                               C
Insecta--Lepidoptera (Moths)                     C
Insecta--Trichoptera (Caddisflies)               B
Insecta--Trichoptera                             B
Insecta--Trichoptera                             B
Insecta--Trichoptera                             B
Insecta--Trichoptera                             B

TABLE 2.--Size range and condition of shells for gastropod
taxa that were consumed and enumerable from wild-caught black
carp diets, 2009-2017. Fish size is reported as total length
in millimeters along with capture dale. Snail size was measured
in millimeters as distance between spire and edge of aperture
opening, with percent fragmentation approximated based on the
proportion of whole shells of the same taxon that were
fragmented or crushed

Fish capture location              Total      Fish
                                   length   capture
                                    (mm)      date

Kaskaskia River, II.                484     8/19/15
Mississippi River, MO               757     12/9/17
  (Pool 26 near Dresser Island)
Lake Ferguson, MS                   803     11/18/16
  (Mississippi River oxbow lake)
Lake Ferguson, MS                   690     11/26/16
  (Mississippi River oxbow lake)
Paradise Lake, MS                   737     1/18/17
  (connecting chute)
Paradise Lake, MS                   831     1/31/17
Horseshoe Lake, AR                  689     7/13/17
  (White River National Fish &
  Wildlife Refuge)
Barkley Lake, KY                    960     11/29/17

Fish capture location              Snail size   Count    Percent
                                   range (mm)           fragmented
                                                        or crushed

Kaskaskia River, II.                  8-21       10         80
Mississippi River, MO                 8-28       67         0
  (Pool 26 near Dresser Island)
Lake Ferguson, MS                     3-26       29         27
  (Mississippi River oxbow lake)
Lake Ferguson, MS                     8-25        9         65
  (Mississippi River oxbow lake)
Paradise Lake, MS                     7-24       23         26
  (connecting chute)
Paradise Lake, MS                     6-25       30         40
Horseshoe Lake, AR                    3-28       25         28
  (White River National Fish &
  Wildlife Refuge)
Barkley Lake, KY                      9-24       69         3

Fish capture location              Snail taxon

Kaskaskia River, II.               Pletiroceridae
Mississippi River, MO              Pleurocera acuta gp.
  (Pool 26 near Dresser Island)
Lake Ferguson, MS                  Vivipanis, V. subpurpureous
  (Mississippi River oxbow lake)
Lake Ferguson, MS                  Viviparus, V. subpurpureous
  (Mississippi River oxbow lake)
Paradise Lake, MS                  Viviparus, V. subpurpureous
  (connecting chute)
Paradise Lake, MS                  Viviparus, V. subpurpureous
Horseshoe Lake, AR                 Vivipams, V. subpuipureous
  (White River National Fish &
  Wildlife Refuge)
Barkley Lake, KY                   Viviparus subpurpureous

TABLE 3.--List of individual wild-caught black carp captured
in 2009-2017 that consumed freshwater unionid mussel species.
Identification of mussels was confirmed from examination of
diet samples with shell fragments possessing diagnostic features
(those lacking diagnostic characters were identified to family).
Fish size is reported as total length in millimeters along with
capture date

Fish capture location                           Total      Fish
                                                length   capture
                                                 (mm)      date

Mississippi River, near Chester, IL              834     1/26/13

Cross Slough, KY (Ohio River drainage)           448      8/2/16

Paradise Lake, MS                                831     1/31/17
(Mississippi River oxbow lake)

Mississippi River, MO, near                      1050    5/15/17
Meramec River confluence

Mississippi River, IL                            1157    5/30/17
(south of St. Louis, MO)

Horseshoe Lake, AR                               689     7/13/17
(While River National Fish & Wildlife Refuge)

Mississippi River, MO, near                      580      8/1/16
Clarksville Island

Mississippi River, IL, at Maple Island           615     8/13/16

Minor Lake, KY                                   674     10/3/16

Lake Ferguson, MS                                803     11/18/16
(Mississippi River oxbow lake)

Lake Ferguson, MS                                690     11/26/16
(Mississippi River oxbow lake)

Lower Mississippi River, MS                      888     6/27/17

Lower Mississippi River, AR                      934     11/14/17

Mississippi River near Tiptonville, TN           941     11/27/17

Little Lake Ferguson, MS                         925     11/30/17
(Mississippi River oxbow)

Fish capture location                           Mussel taxa

Mississippi River, near Chester, IL             Leptodea fragilis

Cross Slough, KY (Ohio River drainage)          Pyganodon grandis

Paradise Lake, MS                               Arcidens confragosus
(Mississippi River oxbow lake)                  Toxolasma parvum

Mississippi River, MO, near                     Pyganodon grandis
Meramec River confluence

Mississippi River, IL                           Leptodea fragilis
(south of St. Louis, MO)                        Potamilus alatus
                                                Pyganodon grandis

Horseshoe Lake, AR                              Leptodea fragilis
(While River National Fish & Wildlife Refuge)   Pyganodon grandis
                                                Toxolasma lividum
                                                Toxolasma

Mississippi River, MO, near                     Unionidae
Clarksville Island

Mississippi River, IL, at Maple Island          Unionidae

Minor Lake, KY                                  Unionidae

Lake Ferguson, MS                               Unionidae
(Mississippi River oxbow lake)

Lake Ferguson, MS                               Unionidae
(Mississippi River oxbow lake)

Lower Mississippi River, MS                     Unionidae

Lower Mississippi River, AR                     Unionidae

Mississippi River near Tiptonville, TN          Unionidae

Little Lake Ferguson, MS                        Unionidae
(Mississippi River oxbow)

TABLE 4.--Identification and quantification of aquatic midges
(Chironomidae) found in the diet of wild-caught black carp
captured in ffoodplain (lenlip=F) and riverine (lotic=R) habitats
in ihe Mississippi River drainage in 2009-2017. Fish size is
reported as total length in millimeters along with capture date,
taxa, and aquatic midge abundance (count)

Fisli capture location                Total      Fish
                                      length   capture
                                       (mm)      date

Lower Sunk Lake, LA                    643       2/09

Cross Slough, KY                       448      8/2/16

Minor Lake, KY                         674     10/3/16

Lake Ferguson, MS                      760     11/18/16
(Mississippi River oxbow lake)

Lake Ferguson, MS                      803     11/18/16
(Mississippi River oxbow lake)

Paradise Lake, MS                      831     1/31/17
(Mississippi River oxbow lake)

Buttonland Swamp, IL                   580     3/28/17

Lee Lake, MS                           776      7/3/17

Horseshoe Lake, AR                     689     7/13/17
(White River National Fish &
Wildlife Refuge)

Little Lake Ferguson, MS               925     11/30/17
(Mississippi River oxbow)

Mississippi River, near Chester, IL    862     1/30/14

Mississippi River, near Alton, IL      573     6/16/16

Mississippi River, MO, near            1280    9/17/16
Maple Island

Mississippi River, MO, near            1050    5/15/17
Meramec River Confluence

Kaskaskia River, IL                    603     6/10/17

Fisli capture location                Habitat   Count

Lower Sunk Lake, LA                      F      > 100

Cross Slough, KY                         F      > 100

Minor Lake, KY                           F      > 100

Lake Ferguson, MS                        F      4
(Mississippi River oxbow lake)

Lake Ferguson, MS                        F      1 (each)
(Mississippi River oxbow lake)

Paradise Lake, MS                        F      1 (each)
(Mississippi River oxbow lake)

Buttonland Swamp, IL                     F      > 100

Lee Lake, MS                             F      > 100

Horseshoe Lake, AR                       F      1
(White River National Fish &
Wildlife Refuge)

Little Lake Ferguson, MS                 F      1
(Mississippi River oxbow)

Mississippi River, near Chester, IL      R      1

Mississippi River, near Alton, IL        R      1

Mississippi River, MO, near              R      1
Maple Island

Mississippi River, MO, near              R      1
Meramec River Confluence

Kaskaskia River, IL                      R      1

Fisli capture location                Taxa

Lower Sunk Lake, LA                   Glyptotendipes, Dicrotendipes

Cross Slough, KY                      Glyptotendipes, Dicrotendipes

Minor Lake, KY                        Glyplolendipes, Diirotmdipes

Lake Ferguson, MS                     Glyptotendipes
(Mississippi River oxbow lake)

Lake Ferguson, MS                     Glyptotendipes, Coelotanypus
(Mississippi River oxbow lake)

Paradise Lake, MS                     Glyptotendipes, Chironomus
(Mississippi River oxbow lake)

Buttonland Swamp, IL                  Glyptotendipes, Dicrotendipes

Lee Lake, MS                          Glyptotendipes, Dicrotendipes

Horseshoe Lake, AR                    Axarus
(White River National Fish &
Wildlife Refuge)

Little Lake Ferguson, MS              Dicrotendipes
(Mississippi River oxbow)

Mississippi River, near Chester, IL   Chironomus

Mississippi River, near Alton, IL     Chironomidae

Mississippi River, MO, near           Chironomidae
Maple Island

Mississippi River, MO, near           PolypedHum
Meramec River Confluence

Kaskaskia River, IL                   Snetheria

FIG. 4.--Percent incidence (n=109) of 11 taxonomic groups of diet
items consumed by wild-caught black carp captured in the
Mississippi River basin from 2009-2017. Number above each bar
represents the total number of distinct taxa within each group

All
Mollusks      21
Unionids      6
Dreissena     1
Corbicula     2
All
Gastropods    10
Viviparidae   2
All
Insects       27
Caddisflies   5
Mayflies      5
Chironomids   9
Other
Taxa          11

Note: Table made from bar graph.
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Author:Poulton, B.C.; Kroboth, P.T.; George, A.E.; Chapman, D.C.; Bailey, J.; McMurray, S.E.; Faiman, J.S.
Publication:The American Midland Naturalist
Article Type:Report
Geographic Code:1USA
Date:Jul 1, 2019
Words:8920
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